The orangutan is the world's largest arboreal mammal, and images of the red ape moving through the tropical forest canopy symbolise its typical arboreal behaviour. Records of terrestrial behaviour are scarce and often associated with habitat disturbance. We conducted a large-scale species-level analysis of ground-based camera-trapping data to evaluate the extent to which Bornean orangutans Pongo pygmaeus come down from the trees to travel terrestrially, and whether they are indeed forced to the ground primarily by anthropogenic forest disturbances. Although the degree of forest disturbance and canopy gap size influenced terrestriality, orangutans were recorded on the ground as frequently in heavily degraded habitats as in primary forests. Furthermore, all age-sex classes were recorded on the ground (flanged males more often). This suggests that terrestrial locomotion is part of the Bornean orangutan's natural behavioural repertoire to a much greater extent than previously thought, and is only modified by habitat disturbance. The capacity of orangutans to come down from the trees may increase their ability to cope with at least smaller-scale forest fragmentation, and to cross moderately open spaces in mosaic landscapes, although the extent of this versatility remains to be investigated.
Anthropogenic habitat disturbance is a major threat to biodiversity worldwide. Yet, before population declines are detectable, individuals may suffer from chronic stress and impaired immunity in disturbed habitats, making them more susceptible to pathogens and adverse weather conditions. Here, we tested in a paleotropical forest with ongoing logging and fragmentation, whether habitat disturbance influences the body mass and immunity of bats. We measured and compared body mass, chronic stress (indicated by neutrophil to lymphocyte ratios) and the number of circulating immune cells between several bat species with different roost types living in recovering areas, actively logged forests, and fragmented forests in Sabah, Malaysia. In a cave-roosting species, chronic stress levels were higher in individuals from fragmented habitats compared with conspecifics from actively logged areas. Foliage-roosting species showed a reduced body mass and decrease in total white blood cell counts in actively logged areas and fragmented forests compared with conspecifics living in recovering habitats. Our study highlights that habitat disturbance may have species-specific effects on chronic stress and immunity in bats that are potentially related to the roost type. We identified foliage-roosting species as particularly sensitive to forest habitat deterioration. These species may face a heightened extinction risk in the near future if anthropogenic habitat alterations continue.
Emerging infectious diseases (EIDs) are considered a major threat to global health. Most EIDs appear to result from increased contact between wildlife and humans, especially when humans encroach into formerly pristine habitats. Habitat deterioration may also negatively affect the physiology and health of wildlife species, which may eventually lead to a higher susceptibility to infectious agents and/or increased shedding of the pathogens causing EIDs. Bats are known to host viruses closely related to important EIDs. Here, we tested in a paleotropical forest with ongoing logging and fragmentation, whether habitat disturbance influences the occurrence of astro- and coronaviruses in eight bat species. In contrast to our hypothesis, anthropogenic habitat disturbance was not associated with corona- and astrovirus detection rates in fecal samples. However, we found that bats infected with either astro- or coronaviruses were likely to be coinfected with the respective other virus. Additionally, we identified two more risk factors influencing astrovirus shedding. First, the detection rate of astroviruses was higher at the beginning of the rainy compared to the dry season. Second, there was a trend that individuals with a poor body condition had a higher probability of shedding astroviruses in their feces. The identification of risk factors for increased viral shedding that may potentially result in increased interspecies transmission is important to prevent viral spillovers from bats to other animals, including humans.
Invertebrates are dominant species in primary tropical rainforests, where their abundance and diversity contributes to the functioning and resilience of these globally important ecosystems. However, more than one-third of tropical forests have been logged, with dramatic impacts on rainforest biodiversity that may disrupt key ecosystem processes. We find that the contribution of invertebrates to three ecosystem processes operating at three trophic levels (litter decomposition, seed predation and removal, and invertebrate predation) is reduced by up to one-half following logging. These changes are associated with decreased abundance of key functional groups of termites, ants, beetles and earthworms, and an increase in the abundance of small mammals, amphibians and insectivorous birds in logged relative to primary forest. Our results suggest that ecosystem processes themselves have considerable resilience to logging, but the consistent decline of invertebrate functional importance is indicative of a human-induced shift in how these ecological processes operate in tropical rainforests.
The conversion of forest to agriculture continues to contribute to the loss and fragmentation of remaining orang-utan habitat. There are still few published estimates of orang-utan densities in these heavily modified agricultural areas to inform range-wide population assessments and conservation strategies. In addition, little is known about what landscape features promote orang-utan habitat use. Using indirect nest count methods, we implemented surveys and estimated population densities of the Northeast Bornean orang-utan (Pongo pygmaeus morio) across the continuous logged forest and forest remnants in a recently salvage-logged area and oil palm plantations in Sabah, Malaysian Borneo. We then assessed the influence of landscape features and forest structural metrics obtained from LiDAR data on estimates of orang-utan density. Recent salvage logging appeared to have a little short-term effect on orang-utan density (2.35 ind/km 2 ), which remained similar to recovering logged forest nearby (2.32 ind/km 2 ). Orang-utans were also present in remnant forest patches in oil palm plantations, but at significantly lower numbers (0.82 ind/km 2 ) than nearby logged forest and salvage-logged areas. Densities were strongly influenced by variation in canopy height but were not associated with other potential covariates. Our findings suggest that orang-utans currently exist, at least in the short-term, within human-modified landscapes, providing that remnant forest patches remain. We urge greater recognition of the role that these degraded habitats can have in supporting orang-utan populations, and that future range-wide analyses and conservation strategies better incorporate data from human-modified landscapes.
Old-growth tropical forests are widely recognized as being immensely important for their biodiversity and high biomass1. Conversely, logged tropical forests are usually characterized as degraded ecosystems2. However, whether logging results in a degradation in ecosystem functions is less clear: shifts in the strength and resilience of key ecosystem processes in large suites of species have rarely been assessed in an ecologically integrated and quantitative framework. Here we adopt an ecosystem energetics lens to gain new insight into the impacts of tropical forest disturbance on a key integrative aspect of ecological function: food pathways and community structure of birds and mammals. We focus on a gradient spanning old-growth and logged forests and oil palm plantations in Borneo. In logged forest there is a 2.5-fold increase in total resource consumption by both birds and mammals compared to that in old-growth forests, probably driven by greater resource accessibility and vegetation palatability. Most principal energetic pathways maintain high species diversity and redundancy, implying maintained resilience. Conversion of logged forest into oil palm plantation results in the collapse of most energetic pathways. Far from being degraded ecosystems, even heavily logged forests can be vibrant and diverse ecosystems with enhanced levels of ecological function.
Tropical forest ecosystems are facing unprecedented levels of degradation, severely compromising habitat suitability for wildlife. Despite the fundamental role biodiversity plays in forest regeneration, identifying and prioritizing degraded forests for restoration or conservation, based on their wildlife value, remains a significant challenge. Efforts to characterize habitat selection are also weakened by simple classifications of human-modified tropical forests as intact vs. degraded, which ignore the influence that three-dimensional (3D) forest structure may have on species distributions. Here, we develop a framework to identify conservation and restoration opportunities across logged forests in Borneo. We couple high-resolution airborne light detection and ranging (LiDAR) and camera trap data to characterize the response of a tropical mammal community to changes in 3D forest structure across a degradation gradient. Mammals were most responsive to covariates that accounted explicitly for the vertical and horizontal characteristics of the forest and actively selected structurally complex environments comprising tall canopies, increased plant area index throughout the vertical column, and the availability of a greater diversity of niches. We show that mammals are sensitive to structural simplification through disturbance, emphasizing the importance of maintaining and enhancing structurally intact forests. By calculating occurrence thresholds of species in response to forest structural change, we identify areas of degraded forest that would provide maximum benefit for multiple high-conservation value species if restored. The study demonstrates the advantages of using LiDAR to map forest structure, rather than relying on overly simplistic classifications of human-modified tropical forests, for prioritizing regions for restoration.
Pollution with pesticides is a widespread global problem and biomonitoring of the environment and human populations is necessary to assess potential harmful biological effects. One of the pesticides that are showing up in vegetables and fruit is chlorpyrifos (CPS). CPS is a nerve-poisoning organophosphorus insecticide, which is in up to 1/3 of all conventionally produced citrus fruits. Our review shows that CPS is a hazardous material that poses risks to human health and also pollutes the environment. There is numerous risk assessment of CPS reported, however, the assessment is easily affected by factors such as climate change, exposure period and CPS concentration. Therefore, rigorous update of the hazardous level of CPS is needed to determine the threshold level safe for humans and animals. There is a need for remediation using for example photoreactive nanoparticle methods and microbial degeneration possessing high degradation efficiency (73-97%). In addition, stringent biomonitoring of food, environment and human exposure should occur to avoid exposure to chemicals via citrus fruits and vegetables. This is necessary to assess health risks and socioeconomic impacts which also require collaboration between private and public sectors to facilitate the growth, sale and manufacturing of biopesticides.
Global warming is reducing the Arctic sea-ice and causing energetic stress to marine key predatory species such as polar bears and narwhals contributing to the ongoing pollution already threatening the biodiversity and indigenous people of the vulnerable region. Now, the opening of the Arctic gateway and in particular the increase in shipping activities causes further stress to marine mammals in the region. These shipping activities are foreseen to happen in the Northwest and Northeast Passage, Northern Sea Route and Transpolar Sea Route in the Arctic Ocean, which could be yet another step towards a crucial tipping point destabilizing global climate, including weathering systems and sea-level rise. This calls for international governance through the establishment of Arctic International National Parks and more Marine Protected Areas through the Arctic Council and UN's Law of the Sea to ensure sustainable use of the Arctic Ocean and adjacent waters.
The island of Borneo is a global biodiversity hotspot. However, its limestone caves are one of its least-studied ecosystems. We report for the first time the fungal species richness, diversity and abundance from Madai cave, situated in north-eastern Borneo. Environmental samples from inside the cave environment were collected (guano, speleothem, and cavern water) via opportunistic sampling. The dilution method was performed for isolation of fungi. Morphological characterisation and molecular analysis of the ITS region were utilised for the identification of isolates. Fifty-five pure cultures of fungi were attained, comprising 32 species from 15 genera, eight orders, and two divisions, Ascomycota and Basidiomycota. Ascomycetes dominated the fungal composition, accounting for 53 (96%) out of 55 total isolates. Penicillium spp. accounted for more than 47.1% of fungal abundance in all sample types. However, Aspergillus spp. had the highest occurrence rate, being isolated from all environmental samples except one. Purpureocillium lilacinum was isolated most frequently, appearing in five separate samples across all three substrates. Annulohypoxylon nitens, Ganoderma australe, Pyrrhoderma noxium, and Xylaria feejeensis were discovered and reported for the first time from the cave environment. This study provides additional data for further research on the mycoflora of Sabah's various ecosystems, especially limestone caves.
The application of metabarcoding to environmental and invertebrate-derived DNA (eDNA and iDNA) is a new and increasingly applied method for monitoring biodiversity across a diverse range of habitats. This approach is particularly promising for sampling in the biodiverse humid tropics, where rapid land-use change for agriculture means there is a growing need to understand the conservation value of the remaining mosaic and degraded landscapes. Here we use iDNA from blood-feeding leeches (Haemadipsa picta) to assess differences in mammalian diversity across a gradient of forest degradation in Sabah, Malaysian Borneo. We screened 557 individual leeches for mammal DNA by targeting fragments of the 16S rRNA gene and detected 14 mammalian genera. We recorded lower mammal diversity in the most heavily degraded forest compared to higher quality twice logged forest. Although the accumulation curves of diversity estimates were comparable across these habitat types, diversity was higher in twice logged forest, with more taxa of conservation concern. In addition, our analysis revealed differences between the community recorded in the heavily logged forest and that of the twice logged forest. By revealing differences in mammal diversity across a human-modified tropical landscape, our study demonstrates the value of iDNA as a noninvasive biomonitoring approach in conservation assessments.
The application of high-throughput sequencing (HTS) for metabarcoding of mixed samples offers new opportunities in conservation biology. Recently, the successful detection of prey DNA from the guts of leeches has raised the possibility that these, and other blood-feeding invertebrates, might serve as useful samplers of mammals. Yet little is known about whether sympatric leech species differ in their feeding preferences, and whether this has a bearing on their relative suitability for monitoring local mammalian diversity. To address these questions, we collected spatially matched samples of two congeneric leech species Haemadipsa picta and Haemadipsa sumatrana from lowland rainforest in Borneo. For each species, we pooled ~500 leeches into batches of 10 individuals, performed PCR to target a section of the mammalian 16S rRNA locus and undertook sequencing of amplicon libraries using an Illumina MiSeq. In total, we identified sequences from 14 mammalian genera, spanning nine families and five orders. We found greater numbers of detections, and higher diversity of OTUs, in H. picta compared with H. sumatrana, with rodents only present in the former leech species. However, comparison of samples from across the landscape revealed no significant difference in mammal community composition between the leech species. We therefore suggest that H. picta is the more suitable iDNA sampler in this degraded Bornean forest. We conclude that the choice of invertebrate sampler can influence the detectability of different mammal groups and that this should be accounted for when designing iDNA studies.
The PREDICTS project-Projecting Responses of Ecological Diversity In Changing Terrestrial Systems (www.predicts.org.uk)-has collated from published studies a large, reasonably representative database of comparable samples of biodiversity from multiple sites that differ in the nature or intensity of human impacts relating to land use. We have used this evidence base to develop global and regional statistical models of how local biodiversity responds to these measures. We describe and make freely available this 2016 release of the database, containing more than 3.2 million records sampled at over 26,000 locations and representing over 47,000 species. We outline how the database can help in answering a range of questions in ecology and conservation biology. To our knowledge, this is the largest and most geographically and taxonomically representative database of spatial comparisons of biodiversity that has been collated to date; it will be useful to researchers and international efforts wishing to model and understand the global status of biodiversity.
Vertebrate granivores destroy plant seeds, but whether animal-induced seed mortality alters plant recruitment varies with habitat context, seed traits, and among granivore species. An incomplete understanding of seed predation makes it difficult to predict how widespread extirpations of vertebrate granivores in tropical forests might affect tree communities, especially in the face of habitat disturbance. Many tropical forests are simultaneously affected by animal loss as well as habitat disturbance, but the consequences of each for forest regeneration are often studied separately or additively, and usually on a single plant demographic stage. The combined impacts of these threats could affect plant recruitment in ways that are not apparent when studied in isolation. We used wire cages to exclude large (elephants), medium, (sambar deer, bearded pigs, muntjac deer), and small (porcupines, chevrotains) ground-dwelling mammalian granivores and herbivores in logged and unlogged forests in Malaysian Borneo. We assessed the interaction between habitat disturbance (selective logging) and experimental defaunation on seed survival, germination, and seedling establishment in five dominant dipterocarp tree species spanning a 21-fold gradient in seed size. Granivore-induced seed mortality was consistently higher in logged forest. Germination of unpredated seeds was reduced in logged forest and in the absence of small to large-bodied mammals. Experimental defaunation increased germination and reduced seed removal but had little effect on seed survival. Seedling recruitment however, was more likely where logging and animal loss occurred together. The interacting effects of logging and hunting could therefore, actually increase seedling establishment, suggesting that the loss of mammals in disturbed forest could have important consequences for forest regeneration and composition.
Orangutans have a long period of immaturity and the longest inter-birth interval (IBI) of all mammals, which can be explained by their solitary life style, preventing the mother from rearing two offspring simultaneously (solitary life hypothesis) [corrected]. We collected data on mother-offspring dyads living in a primary lowland forest in Danum Valley, East Borneo in an effort to examine the developmental and behavioral patterns of the subspecies Pongo pygmaeus morio. We analyzed developmental changes in mother-offspring distance, contact, and activity budgets in orangutans ranging from 1 to 7 years of age. The results indicated decreased resting and playing with increasing age, whereas feeding, traveling and social play all increased significantly. Mothers' feeding and traveling time were good predictors of their offspring's feeding and traveling activities. Mother-offspring contact lasted longer in resting contexts; contact during traveling was almost non-existent after 4 years of age. Comparisons with previously published data on the Sumatran species Pongo abelli revealed no fundamental differences in these behavioral measures. However, a shorter association time with the mother after behavioral independence is documented for this East Bornean population in comparison to Sumatran populations. These results are best explained by the solitary life hypothesis, in agreement with previous studies. We suggest that environmental constraints in Bornean forests, as well as a lower population density, should be considered when interpreting the differences between Sumatran and Bornean orangutans in both the period of association with mother and the IBI.
Many species of terrestrial animals, including primates, live in varied association with the aquatic (e.g., riverine or coastal) environment. However, the benefits that each species receive from the aquatic environment are thought to vary depending on their social and ecological characteristics, and thus, elucidating those benefits to each species is important for understanding the principles of wild animal behaviour. In the present study, to gain a more complete picture of aquatic environment use, including social and ecological factors in primates, factors affecting riverine habitat utilization of two macaque species (Macaca nemestrina and M. fascicularis) were identified and qualitative comparisons were made with sympatric proboscis monkeys (Nasalis larvatus), which have different social and ecological characteristics. Temporal variation in sighting frequency of macaques at the riverbanks was positively related to the fruit availability of a dominant riparian plant species and negatively related to the river water level which affects the extent of predation pressure. Riverine utilization of macaques was greatly influenced by distribution and abundance of food (especially fruit) resources, possibly in association with predation pressure. Additionally, qualitative ecological comparisons with sympatric proboscis monkeys suggest that the drivers of riverine utilization depend on the feeding niches of the species, and different anti-predator strategies resulting from their differing social structures.
The marbled cat Pardofelis marmorata is a poorly known wild cat that has a broad distribution across much of the Indomalayan ecorealm. This felid is thought to exist at low population densities throughout its range, yet no estimates of its abundance exist, hampering assessment of its conservation status. To investigate the distribution and abundance of marbled cats we conducted intensive, felid-focused camera trap surveys of eight forest areas and two oil palm plantations in Sabah, Malaysian Borneo. Study sites were broadly representative of the range of habitat types and the gradient of anthropogenic disturbance and fragmentation present in contemporary Sabah. We recorded marbled cats from all forest study areas apart from a small, relatively isolated forest patch, although photographic detection frequency varied greatly between areas. No marbled cats were recorded within the plantations, but a single individual was recorded walking along the forest/plantation boundary. We collected sufficient numbers of marbled cat photographic captures at three study areas to permit density estimation based on spatially explicit capture-recapture analyses. Estimates of population density from the primary, lowland Danum Valley Conservation Area and primary upland, Tawau Hills Park, were 19.57 (SD: 8.36) and 7.10 (SD: 1.90) individuals per 100 km2, respectively, and the selectively logged, lowland Tabin Wildlife Reserve yielded an estimated density of 10.45 (SD: 3.38) individuals per 100 km2. The low detection frequencies recorded in our other survey sites and from published studies elsewhere in its range, and the absence of previous density estimates for this felid suggest that our density estimates may be from the higher end of their abundance spectrum. We provide recommendations for future marbled cat survey approaches.
Information on tropical Asian vertebrates has traditionally been sparse, particularly when it comes to cryptic species inhabiting the dense forests of the region. Vertebrate populations are declining globally due to land-use change and hunting, the latter frequently referred as "defaunation." This is especially true in tropical Asia where there is extensive land-use change and high human densities. Robust monitoring requires that large volumes of vertebrate population data be made available for use by the scientific and applied communities. Camera traps have emerged as an effective, non-invasive, widespread, and common approach to surveying vertebrates in their natural habitats. However, camera-derived datasets remain scattered across a wide array of sources, including published scientific literature, gray literature, and unpublished works, making it challenging for researchers to harness the full potential of cameras for ecology, conservation, and management. In response, we collated and standardized observations from 239 camera trap studies conducted in tropical Asia. There were 278,260 independent records of 371 distinct species, comprising 232 mammals, 132 birds, and seven reptiles. The total trapping effort accumulated in this data paper consisted of 876,606 trap nights, distributed among Indonesia, Singapore, Malaysia, Bhutan, Thailand, Myanmar, Cambodia, Laos, Vietnam, Nepal, and far eastern India. The relatively standardized deployment methods in the region provide a consistent, reliable, and rich count data set relative to other large-scale pressence-only data sets, such as the Global Biodiversity Information Facility (GBIF) or citizen science repositories (e.g., iNaturalist), and is thus most similar to eBird. To facilitate the use of these data, we also provide mammalian species trait information and 13 environmental covariates calculated at three spatial scales around the camera survey centroids (within 10-, 20-, and 30-km buffers). We will update the dataset to include broader coverage of temperate Asia and add newer surveys and covariates as they become available. This dataset unlocks immense opportunities for single-species ecological or conservation studies as well as applied ecology, community ecology, and macroecology investigations. The data are fully available to the public for utilization and research. Please cite this data paper when utilizing the data.